Object and place memory in the macaque entorhinal cortex

Lesions of the entorhinal cortex in humans, monkeys, and rats impair memory for a variety of kinds of information, including memory for objects and places. To begin to understand the contribution of entorhinal cells to different forms of memory, responses of entorhinal cells were recorded as monkeys performed either an object or place memory task. The object memory task was a variation of delayed matching to sample. A sample picture was presented at the start of the trial, followed by a variable sequence of zero to four test pictures, ending with a repetition of the sample (i.e., a match). The place memory task was a variation of delayed matching to place. In this task, a cue stimulus was presented at a variable sequence of one to four "places" on a computer screen, ending with a repetition of one of the previously shown places (i.e., a match). For both tasks, the animals were rewarded for releasing a bar to the match. To solve these tasks, the monkey must 1) discriminate the stimuli, 2) maintain a memory of the appropriate stimuli during the course of the trial, and 3) evaluate whether a test stimulus matches previously presented stimuli. The responses of entorhinal cortex neurons were consistent with a role in all three of these processes in both tasks. We found that 47% and 55% of the visually responsive entorhinal cells responded selectively to the different objects or places presented during the object or place task, respectively. Similar to previous findings in prefrontal but not perirhinal cortex on the object task, some entorhinal cells had sample-specific delay activity that was maintained throughout all of the delay intervals in the sequence. For the place task, some cells had location-specific maintained activity in the delay immediately following a specific cue location. In addition, 59% and 22% of the visually responsive cells recorded during the object and place task, respectively, responded differently to the test stimuli according to whether they were matching or non-matching to the stimuli held in memory. Responses of some cells were enhanced to matching stimuli, whereas others were suppressed. This suppression or enhancement typically occurred well before the animals' behavioral response, suggesting that this information could be used to perform the task. These results indicate that entorhinal cells receive sensory information about both objects and spatial locations and that their activity carries information about objects and locations held in short-term memory.     

Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1

We examined the responsivity, orientation selectivity, and direction selectivity of a sample of neurons in cortical area V1 of the macaque using visual stimuli consisting of drifting oriented contours defined by each of two very different figural cues: luminance contrast and temporal texture. Comparisons of orientation and direction tuning elicited by the different cues were made in order to test the hypothesis that the neuronal representations of these parameters are form-cue invariant. The majority of the sampled cells responded to both stimulus types, although responses to temporal texture stimuli were generally weaker than those elicited by luminance-defined stimuli. Of those units exhibiting orientation selectivity when tested with the luminance-defined stimuli, more than half were also selective for the orientation of the temporal texture stimuli. There was close correspondence between the preferred orientations and tuning bandwidths revealed with the two stimulus types. Of those units exhibiting directional selectivity when tested with the luminance-defined stimuli, about two-thirds were also selective for the direction of the temporal texture stimuli. There was close correspondence between the preferred directions revealed with the two stimulus types, although bidirectional responses were somewhat more common when temporal texture stimuli were used. These results indicate that many V1 neurons encode orientation and direction of motion of retinal image features in a manner that is largely independent of whether the feature is defined by luminance or temporal texture contrast. These neurons may contribute to perceptual phenomena in which figural cue identity is disregarded.     

Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate

When visuospatial stimuli instruct a limb movement, the stimulus can be said to have both sensory and sensorimotor aspects. We studied the premotor and prefrontal areas of a rhesus monkey in order to identify neuronal activity related to the motor (or instructional) aspects of such stimuli. A rhesus monkey chose limb-movement targets according to one of two rules: (1) visuospatial stimuli instructed and triggered a limb movement toward their locations or (2) identical stimuli triggered a movement toward a predetermined target regardless of their location. Gaze and head fixation assured that each stimulus appeared at a constant location in both retinocentric and craniocentric coordinates, as well as in allocentric space. The task required that the spatial location cued by certain stimuli had to be either remembered or attended after stimulus presentation and before movement. Thus, the visuospatial information presented under one rule differed from that presented under the other only in its motor (instructional) significance and not in its attentional, spatial, mnemonic, or strictly sensory aspects. We could thereby test and confirm the hypothesis that the motor significance of visuospatial cues should commonly affect neuronal activity in the premotor cortex, but less commonly do so in the prefrontal cortex.     

The impact of stimulus and response variability on S-R correspondence effects.

Six experiments investigated how variability on irrelevant stimulus dimensions and variability on response dimensions contribute to spatial and nonspatial stimulus-response (S-R) correspondence effects. Experiments 1-3 showed that, when stimuli varied in location and number, S-R correspondence effects for location or numerosity occurred when responses varied on these dimensions but not when responses were invariant on these dimensions. These results are consistent with the response-discrimination account, according to which S-R correspondence effects should only arise for a dimension that is used for discriminating between responses in working memory. Experiments 4-6 showed that, when responses varied in location and number, both invariant and variable stimulus number produced correspondence effects in S-R numerosity. In summary, the present results indicate that the usefulness of a particular dimension for response discrimination can be sufficient for producing S-R correspondence effects, whereas variability of a stimulus dimension is not sufficient for producing such effects. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Processing of contrast polarity of visual images in inferotemporal cortex of the macaque monkey

Cells in the anterior part of the inferotemporal cortex (anterior IT) respond to moderately complex stimulus features of object images. To study dependency of their responses on contrast polarity of stimulus images, we selected cells with optimal stimuli that were defined only by shape and not related to texture or color, and examined effects of reversing the contrast of the image or removing it except for edges between dark and bright parts of the image ("outlining"). The contrast reversal produced a reduction of the response to the optimal stimulus by > 50% in 60% of tested cells; the outlining, in 70%. When the two transformations were considered together, 94% of the cells showed a reduction by > 50%. Effects of the transformations on shape selectivity were also studied by comparing responses to several different shapes each of whose contours were expressed in different ways. Statistically significant changes in relative effectiveness of the different shapes as a function of contour expression were observed in more than half of the cells. These results suggest that responses of individual cells in anterior IT carry information about contrast polarity as well as about shape.     

The influence of stimulus properties on multisensory processing in the awake primate superior colliculus.

Evaluated the influence of physical properties of sensory stimuli (visual intensity, direction, and velocity; auditory intensity and location) on sensory activity and multisensory integration of superior colliculus (SC) neurons in awake, behaving primates. Two male monkeys were trained to fixate a central visual fixation point while visual and/or auditory stimuli were presented in the periphery. Visual stimuli were always presented within the contralateral receptive field of the neuron whereas auditory stimuli were presented at either ipsi- or contralateral locations. 66 of the 84 SC neurons responsive to these sensory stimuli had stronger responses when the visual and auditory stimuli were combined at contralateral locations than when the auditory stimulus was located on the ipsilateral side. This trend was significant across the population of auditory-responsive neurons. In addition, 31 SC neurons were presented a battery of tests in which the quality of one stimulus of a pair was systematically manipulated. Eight of these neurons showed preferential responses to stimuli with specific physical properties, and these preferences were not significantly altered when multisensory stimulus combinations were presented. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Spatial frequency discrimination: visual long-term memory or criterion setting?

A long-term sensory memory is believed to account for spatial frequency discrimination when reference and test stimuli are separated by long intervals. We test an alternative proposal: that discrimination is determined by the range of test stimuli, through their entrainment of criterion-setting processes. Experiments 1 and 2 show that the 50% point of the psychometric function is largely determined by the midpoint of the stimulus range, not by the reference stimulus. Experiment 3 shows that discrimination of spatial frequencies is similarly affected by orthogonal contextual stimuli and parallel contextual stimuli and that these effects can be explained by criterion-setting processes. These findings support the hypothesis that discrimination over long intervals is explained by the operation of criterion-setting processes rather than by long-term sensory retention of a neural representation of the stimulus.     

Auditory-visual cross-modal perception of communicative stimuli in Tufted Capuchin Monkeys (Cebus apella).

Research on cross-modal performance in nonhuman primates is limited to a small number of sensory modalities and testing methods. To broaden the scope of this research, the authors tested capuchin monkeys (Cebus apella) for a seldom-studied cross-modal capacity in nonhuman primates, auditory-visual recognition. Monkeys were simultaneously played 2 video recordings of a face producing different vocalizations and a sound recording of 1 of the vocalizations. Stimulus sets varied from naturally occurring conspecific vocalizations to experimentally controlled human speech stimuli. The authors found that monkeys preferred to view face recordings that matched presented vocal stimuli. Their preference did not differ significantly across stimulus species or other stimulus features. However, the reliability of the latter set of results may have been limited by sample size. From these results, the authors concluded that capuchin monkeys exhibit auditory-visual cross-modal perception of conspecific vocalizations. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Visual attention mediated by biased competition in extrastriate visual cortex

According to conventional neurobiological accounts of visual attention, attention serves to enhance extrastriate neuronal responses to a stimulus at one spatial location in the visual field. However, recent results from recordings in extrastriate cortex of monkeys suggest that any enhancing effect of attention is best understood in the context of competitive interactions among neurons representing all of the stimuli present in the visual field. These interactions can be biased in favour of behaviourally relevant stimuli as a result of many different processes, both spatial and non-spatial, and both bottom-up and top-down. The resolution of this competition results in the suppression of the neuronal representations of behaviourally irrelevant stimuli in extrastriate cortex. A main source of top-down influence may derive from neuronal systems underlying working memory.     

The Von Restorff effect in visual object recognition memory in humans and monkeys. The role of frontal/perirhinal interaction

This study reports the development of a new, modified delayed matching to sample (DMS) visual recognition memory task that controls the relative novelty of test stimuli and can be used in human and nonhuman primates. We report findings from normal humans and unoperated monkeys, as well as three groups of operated monkeys. In the study phase of this modified paradigm, subjects studied lists of two-dimensional visual object stimuli. In the test phase each studied object was presented again, now paired with a new stimulus (a foil), and the subject had to choose the studied item. In some lists one study item (the novel or isolate item) and its associated foil differed from the others (the homogenous items) along one stimulus dimension (color). The critical experimental measure was the comparison of the visual object recognition error rates for isolate and homogenous test items. This task was initially administered to human subjects and unoperated monkeys. Error rates for both groups were reliably lower for isolate than for homogenous stimuli in the same list position (the von Restorff effect). The task was then administered to three groups of monkeys who had selective brain lesions. Monkeys with bilateral lesions of the amygdata and fornix, two structures that have been proposed to play a role in novelty and memory encoding, were similar to normal monkeys in their performance on this task. Two further groups--with disconnection lesions of the perirhinal cortex and either the prefrontal cortex or the magnocellular mediodorsal thalamus--showed no evidence of a von Restorff effect. These findings are not consistent with previous proposals that the hippocampus and amygdala constitute a general novelty processing network. Instead, the results support an interaction between the perirhinal and frontal cortices in the processing of certain kinds of novel information that support visual object recognition memory.     

Visuo-oculomotor properties of cells in the superior colliculus of the alert cat

Visual responses and eye movement (EM) -related activities were studied in single units of the superior colliculus (SC) of alert cats. Spontaneous EMs were encouraged by training. Throughout the SC (i.e., in intermediate and deep layers as well as in superficial layers), units were found to respond well to visual stimuli. Strong and consistent responses could be elicited by very dim, low-contrast stationary stimuli. Visual responses varied from phasic to tonic; some units responded tonically to stationary stimuli in the center of the receptive field, and phasically to peripheral stimuli. Many cells responded more vigorously to moving than to stationary stimuli, but very few responded exclusively to stimulus movement. The vast majority of cells were directionally selective. A small number of units were sensitive to the absolute, as well as the retinal, position of visual stimuli. These cells were activated by visual stimuli which fell in the receptive field only if the cat's gaze was fixated on one half of the screen. It seems that these cells must receive information about both eye position and the retinal (receptive field) position of the stimulus. It is possible that they reflect coding of target location within a head (or body) frame of reference. EM-related units were of two types: (1) about 20% of the sample responded prior to spontaneous or visually-triggered EMs, and (2) another 10% (or more) responded with, but not before, EMs. Some cells in the second group discharge almost synchronously with EMs and, thus, cannot plausibly be said to respond to the movement of images across the retina. All cells in the first group were directionally selective. The percentage of EM-related cells in the deep layers of SC is lower in cat than in monkey. Possible reasons for such differences are discussed.     

Effects of gaze on apparent visual responses of frontal cortex neurons

Previous reports have argued that single neurons in the ventral premotor cortex of rhesus monkeys (PMv, the ventrolateral part of Brodmann's area 6) typically show spatial response fields that are independent of gaze angle. We reinvestigated this issue for PMv and also explored the adjacent prearcuate cortex (PAv, areas 12 and 45). Two rhesus monkeys were operantly conditioned to press a switch and maintain fixation on a small visual stimulus (0.2 degree x 0.2 degree) while a second visual stimulus (1 degree x 1 degree or 2 degrees x 2 degrees) appeared at one of several possible locations on a video screen. When the second stimulus dimmed, after an unpredictable period of 0.4-1.2 s, the monkey had to quickly release the switch to receive liquid reinforcement. By presenting stimuli at fixed screen locations and varying the location of the fixation point, we could determine whether single neurons encode stimulus location in "absolute space" or any other coordinate system independent of gaze. For the vast majority of neurons in both PMv (90%) and PAv (94%), the apparent response to a stimulus at a given screen location varied significantly and dramatically with gaze angle. Thus, we found little evidence for gaze-independent activity in either PMv or PAv neurons. The present result in frontal cortex resembles that in posterior parietal cortex, where both retinal image location and eye position affect responsiveness to visual stimuli.     

Do pigeons (Columba livia) study for a test?

In 4 experiments, the authors asked whether pigeons (Columba livia) would show metamemory by choosing to study a sample stimulus before taking a memory test. In Experiments 1a–1c, pigeons chose between cues that led either to exposure to a sample stimulus or directly to the comparison test stimuli without seeing the sample in a delayed matching-to-sample task. The same choice was used in Experiment 2 to see whether pigeons would take a reminder when memory of the sample was weak. In Experiments 3 and 4, pigeons’ responses led to either a choice between red and green side keys with a sample present to guide the choice or a choice with no sample present. The findings of all of these experiments suggest the absence of metamemory in pigeons. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Comparative evaluation of two models for estimating sample sizes for tests on trends across repeated measurements

The emotional content of stimuli can enhance memory for those stimuli. This process may occur via an interaction with systems responsible for perception and memory or via the addition of distinct brain regions specialized for emotion which augment mnemonic processing. We performed an 15O PET study to identify neuroanatomical systems which encode visual stimuli with strong negative emotional valence compared to stimuli with neutral valence. Subjects also performed a recognition memory task for these same images, mixed with distracters of similar emotional valence. The experimental design permitted us to independently test effects of emotional content and recognition memory on regional activity. We found activity in the left amygdaloid complex associated with the encoding of emotional stimuli, although this activation appeared early in the scanning session and was not detectable during recognition memory. Visual recognition memory recruited the right middle frontal gyrus and the superior anterior cingulate cortex for both negative and neutral stimuli. An interaction occurred between emotional content and recognition in the lingual gyrus, where greater activation occurred during recognition of negative images compared to recognition of neutral images. Instead of distinct neuroanatomical systems for emotion augmenting memory, we found that emotionally salient stimuli appeared to enhance processing of early sensory input during visual recognition.     

The structure and precision of retinal spike trains

Assessing the reliability of neuronal spike trains is fundamental to an understanding of the neural code. We measured the reproducibility of retinal responses to repeated visual stimuli. In both tiger salamander and rabbit, the retinal ganglion cells responded to random flicker with discrete, brief periods of firing. For any given cell, these firing events covered only a small fraction of the total stimulus time, often less than 5%. Firing events were very reproducible from trial to trial: the timing jitter of individual spikes was as low as 1 msec, and the standard deviation in spike count was often less than 0.5 spikes. Comparing the precision of spike timing to that of the spike count showed that the timing of a firing event conveyed several times more visual information than its spike count. This sparseness and precision were general characteristics of ganglion cell responses, maintained over the broad ensemble of stimulus waveforms produced by random flicker, and over a range of contrasts. Thus, the responses of retinal ganglion cells are not properly described by a firing probability that varies continuously with the stimulus. Instead, these neurons elicit discrete firing events that may be the fundamental coding symbols in retinal spike trains.     

Postexcitatory inhibition of the crayfish lateral giant neuron: a mechanism for sensory temporal filtering

Crayfish escape from threats by either giant neuron-mediated "reflex" tail flexions that occur with very little delay but do not allow for much sensory guidance of trajectory or by "nongiant" tail flexion responses that allow for sensory guidance but occur much less promptly. Thus, when a stimulus occurs, the nervous system must make a rapid assessment of whether to use the faster reflex system or the slower nongiant one. It does this on the basis of the abruptness of stimulus onset; only stimuli of very abrupt onset trigger giant-mediated responses. We report here that stimuli which excite the lateral giant (LG) command neurons for one form of reflex escape also produce a slightly delayed postexcitatory inhibition (PEI) of the command neurons. As a result, only stimuli that become strong enough to excite the command neurons to firing threshold before the onset of PEI, within a few milliseconds of stimulus onset, can cause giant-mediated responses. This inhibition is directed to distal dendrites of the LG neurons, which allows for some location specificity of PEI within the sensory field of a single hemisegment.     

A honeybee's ability to learn, recognize, and discriminate odors depends upon odor sampling time and concentration.

Animals sample sensory stimuli for longer periods when they must perform difficult discrimination tasks, implying that the brain's ability to represent stimuli improves as a function of time. Although it is true in other senses, few studies have examined whether increasing sampling time improves olfactory discrimination. In the experiments reported here, odor sampling time was controlled with the goal of testing whether odor concentration affected a honeybee's ability to learn, recognize, and discriminate odors. Increasing sampling time during conditioning and testing improved a honeybee's ability to learn, recognize, and differentiate low-concentration (0.0002 M) odors. For intermediate-concentration (0.02 M) odors, both acquisition and recognition improved when stimulus duration was longer, but discrimination was unaffected. Having longer to sample a high-concentration (2.0 M) stimulus also improved acquisition, but it did not affect the ability to recognize or differentiate odors. Differences in time to respond to the conditioned and novel odors during the test period depended on the difficulty of the discrimination task. The results suggest that the sensory coding of molecular identity takes longer for low-concentration odors. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

On the relationship between recognition familiarity and perceptual fluency: evidence for distinct mnemonic processes

Fluent reprocessing of perceptual aspects of recently experienced stimuli is thought to support repetition priming effects on implicit perceptual memory tests. Although behavioral and neuropsychological dissociations demonstrate that separable mnemonic processes and neural substrates mediate implicit and explicit test performance, dual-process theories of memory posit that explicit recognition memory judgments may be based on familiarity derived from the same perceptual fluency that yields perceptual priming. Here we consider the relationship between familiarity-based recognition memory and implicit perceptual memory. A select review of the literature demonstrates that the fluency supporting implicit perceptual memory is functionally and anatomically distinct from that supporting recognition memory. In contrast to perceptual fluency, recognition familiarity is more sensitive to conceptual than to perceptual processing, and does not depend on modality-specific sensory cortices. Alternative possible relationships between familiarity in explicit memory and fluency in implicit memory are discussed.     

Binocular rivalry: Central or peripheral selective processes?

The traditionally held notion that binocular rivalry reflects central selective processes that take effect subsequent to the analysis of both monocular stimuli contrasts with the currently popular view that the suppressed stimulus suffers inhibition, or blocking, at a relatively peripheral level. The available evidence supports the traditional approach. It is argued that although peripheral responses such as changes in pupil diameter or accommodation may be correlated with rivalry suppression, they may not be held responsible for the suppression itself. Similarly, processes of adaptation and contralateral inhibition are unable to explain binocular rivalry. There is evidence, however, that the suppressed stimulus in rivalry is being fully analyzed and evaluated. Perceptual experience is thereby shown to reflect processes over and above the analysis of sensory information, and binocular rivalry suggests itself as a useful context in which to isolate and investigate these processes. (105 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Right-hemispheric superiority in split-brain monkeys for learning and remembering facial discriminations

Twenty-six split-brain rhesus monkeys learned and remembered 8 go/no-go discriminations of monkey faces significantly better with the right hemisphere than with the left. Four discriminations required differentiating individual identity with expression held constant, and 4 required discriminating facial expression with identity held constant. There was no significant difference in the degree of laterality shown for these 2 types of problems. Female monkeys were more lateralized for learning to discriminate faces than were males. This sex difference in laterality was significant for learning but not for memory. Laterality for the facial discriminations was not significantly related to handedness of the monkeys. Overall, rhesus monkeys, like humans, show a right-hemispheric superiority for facial processing.